The Destiny Destroyer is in the shape of an enormous green octahedron, similar to the Diamond Communicator. It has a small windscreen on the front, presumably where the cockpit is. Four long, claw-like prongs extend from all four sides of it. The prongs are where the ship's main cannons are located. The ship is also armed with an arsenal of precision missiles. A diamond-shaped thruster is located at the back.
"Lars of the Stars"
Emerald uses the ship to track the Sun Incinerator while Lars and the Off Colors are fleeing Homeworld on board it. Stevonnie, piloting the Star Skipper, destroys the Destiny Destroyer's main cannons, but is shot down by the missiles the ship fires. As the Star Skipper hurtles toward the Jungle Moon, Lars video calls Stevonnie and informs them that the Destiny Destroyer was sent on the run due to the damage it sustained, presumably returning to Homeworld or another Gem base.
- Weapons: The ship can charge and fire energy beams from its prongs, and is further armed with guided missile launchers.
- Sun Incinerator Tracker: The ship can track the movement of Emerald's fastest ship, the Sun Incinerator, through a unique energy signature its Nova Thrusters leave. According to Emerald, this energy signature can be detected even if the two ships are on other sides of a galaxy.
- Communicator: The ship can allow the user to video call another individual.
- The ship's name is very reminiscent of the Imperial Star Destroyers from the Star Wars franchise.